Genetic Analysis of Pere David's x Red Deer
Interspecies Hybrids
M. L. Tate, G. J. Goosen, H. Patene, A. J. Pearse, K. M. McEwan, and
P. F. Fennessy
From the AgResearch Molecular Biology Unit, Department of Biochemistry, University of Otago, P.O. Box 56,
Dunedln, New Zealand (Tate) and AgResearch, Invermay Agricultural Centre, Mosglel, New Zealand (Goosen, Patene, Pearse, McEwan, and Fennessy). We gratefully acknowledge the assistance of other members of
the Invermay deer group and G. W. Asher (or assistance
with the manuscript. This paper was delivered at a
symposium entitled "Interspecies Hybrids In Mammals" In association with the New Zealand Genetlcal
Society and Australasian Gene Mapping Workshop in
Dunedln, New Zealand, from November 30-December
1, 1995.
Journal of Heredity 1997^8^61-365; 0022-1503/97/$5.00
New Zealand has no native deer, but European settlers introduced nine taxa into
a variety of areas from 1851 to 1910 (King
1990). Hybridization has become widespread in some cases. The most prominent examples are hybrid zones between
red deer (Cervus elaphus scoticus) and
North American wapiti (C. e. nelsoni; Nugent et al. 1987) and between red deer and
sika deer (C. nippon; Davidson 1983). During the 1970s large numbers of red deer
and red deer x wapiti hybrids were captured from wild populations for farming.
Hybrids have been used widely in the
breeding of farmed deer, and the production of novel hybrids has been a focus in
strategies for genetic Improvement of
farmed deer (Fennessy et al. 1992). This
has resulted in numerous hybrids between
subspecies of red deer and also the production of much wider interspecies hybrids, including 26 F, hybrids (12 males:14
females) between Pere David's deer (Elaphurus dauidianus') and red deer (Asher et
al. 1988; Fennessy and Mackintosh 1992;
Tate ML, unpublished data) and a single
living hybrid female between red deer and
sambar deer (C. unicolor, Muir et al. 1996).
We have focused our research on Pere
David's deer hybrids because these are
the widest known deer hybrids in which
both sexes of F, hybrid are fertile (Fennessy et al. 1992). The fertility, particularly
of the male F, hybrid, is remarkable given
the large genetic distance, with a Nei's
(1972) D of 0.48 (Tate et al. 1992), and the
biological differences between the species. Pere David's deer are distinct from
red deer in seasonality (Loudon et al.
1989), behavior (Altmann and Scheel 1980;
Bedford 1951), morphology (Wemmer
1983), mature size (Whitehead 1993), and
disease resistance (Orr and Mackintosh
1988). In addition, Pere David's deer differ
from all other living deer in the structure
of their antler (Whitehead 1993). Hybridization was achieved only by artificial insemination (Fennessy and Mackintosh
1992). Natural mating was unsuccessful
because of the difference In breeding season between the species, the lack of social
integration between Pere David's deer and
red deer, and the attrition of Pere David's
deer to malignant catarrhal fever (MCF)
(Orr and Mackintosh 1988).
DNA from backcross pedigrees born in
1990 and 1991 was used to generate genetic maps of some deer chromosomes.
These maps identified the Pere David's
deer backcross DNA panel as a valuable
resource for comparative gene mapping
(Broom et al. 1996; Tate et al. 1995). In this
article we describe our success in using
artificial breeding technology to generate
a large number of additional backcross
Pere David's deer X red deer hybrids. We
361
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Interspecies hybrids provide unique opportunities for fundamental genetic analyses and for genetic improvement of farmed deer. We have bred F, hybrids by artificial insemination of red deer hinds (Cervus elaphus) with semen from Pere David's
deer (Elaphurus davldlanus). The male and female F, Pere David deer x red deer
hybrids were fertile and in matlngs with red deer have produced over 300 viable
backcross hybrids. DNA was collected from the backcross progeny as an International reference panel for gene linkage mapping and to investigate associations
between segregating species-specific genetic markers and phenotyplc traits. We
have measured a range of phenotypic traits in the backcross hybrids and red deer.
Several traits appear suitable for genetic analysis using mapped genetic markers,
including gestation length, growth rate, live weight, head morphometrlcs, and tail
length. Typically these traits show a large difference between Pere David's deer
and red deer and a high variance in the backcross so that many Individuals have
a phenotype outside the range observed in red deer.
Table 1. Interspecle* hybridization among the Cervlnae: comparisons of pregnancy rate (day 40), birth rate, and perinatal death rate
Number
Inseminations
Species
Sire
Dam
Red deer
Red deer
F, Pere David's deer X red deer
F, Pere David's deer x red deer
Wapiti
Red deer
Pere David's deer
Sambar deer
Red deer
Red deer
Red deer
Red deer
Red deer
Red deer
F, Pere David's deer x red deer
Red deer
Red deer
Sambar deer
Breeding
method
or inflt-
Al
Al
Al
140
Natural
Al
MOET'
Al
Al
Al
Ings
841
155
59
52
116
400
10
Hinds
nreonant'
Calves
born
102
167
321
56
39
34
15
31
5
99
164
301
53
36
25
9
4
0
Pregnancies
lost (*)
2.9
2.4
2.4
6.5
7.1'
30
40
87
100
Calves
born
dead
(*)
Reference
18
9
—
24
11
75
—
Fennessy et al. 1991
Cited by Fennessy et al. 1991
This article
This article
Fennessy et al. 1991
This article
Fennessy and Mackintosh 1992
Muir et al. 1996
Mulr et al. 19%
• Pregnancy diagnosis by ultrasound at 32-42 days.
*Red deer recipient dams (multiple ovulation and embryo transfer).
' Includes one set of twins.
Methods
Backcross progeny (1/4 Pere David's deer
x 3/4 red deer) were obtained over a period of 6 years by either natural mating or
artificial insemination (Al) of red deer
hinds (F, hybrid sires) or multiple ovulation and embryo transfer (MOET) using F,
hybrid dams as donors (red deer sire) (Table 1). Semen from six F, hybrid stags was
used in a total of 841 laparoscopic interuterine inseminations (Asher et al. 1993;
Fennessy et al. 1991). In each case, semen
was collected on the day of insemination
by electroejaculation (Asher et al. 1993),
and between 3 x 10s and 30 x 106 live
sperm were inseminated per hind. For natural mating, small groups of hinds (four to
five) in synchronized estrus were presented to a stag every 2-3 days (Fennessy et
al. 1991). For MOET a total of 53 embryos,
obtained from the natural matings of five
superovulated F, hybrid hinds, were transferred to 52 red deer recipients. Superovulation and embryo transfer procedures
followed those outlined by Fennessy et al.
(1994).
All hinds in the natural mating, Al, and
MOET programs were examined by rectal
ultrasonography (Wilson and Bingham
1990) 32 and 42 days after insemination,
or transfer, to assess pregnancy status.
During the calving season, hinds were
monitored daily and newborn calves were
tagged and the birth weight, sex, and dam
3 6 2 The Journal of Heredity 1997.88(5)
identification were recorded. For hinds
that conceived by Al, the date of conception was taken as the Al date, while for
hinds that conceived by synchronized natural mating or embryo transfer, the date
of conception was taken as 72 h after the
withdrawal of progesterone treatment.
Each cohort of backcross hybrid animals
was raised on pasture with a comparison
group comprising a minimum of 30 red
deer. The backcross deer and their contemporary red deer were weighed at least
monthly from weaning until 15 months of
age. The date of antler casting, in late winter/early spring, was recorded during routine animal feeding.
At 15 months of age, animals were sedated and X-ray images were taken of the
skull (dorso-ventral and lateral), the metatarsals, front phalanges and hoof (lateral), and the pelvic and caudal vertebrae
(lateral) using an Atomscope 803 (Mikasa
X-ray Co. Ltd, Tokyo) and X-OMAT-K film
(Kodak, USA) with Lightening Plus screens
(Du-Pont, USA). So to minimize enlargement, all X-rays were taken with 1600 cm
between the source and the film and the
limb placed directly on top of the cassette
containing the film. The following measurements were taken directly from the
X-ray image: skull length (from the posterior point of the supraoccipital to the anterior point of the premaxilla), skull width
at the widest point (behind the orbit),
metatarsal length, foot length (from the
proximal end of the first phalange to the
tip of the third phalange), and tail length
(from the anterior end of the first tail vertebrae not obscured by the rump to the
tip of the last tail vertebrae). For each
measurement, the hypothesis that the
variance was greater in the backcross
than the red deer controls was tested and
the means of the two groups were compared using t tests (variances unequal).
In addition, comparative data on the
timing of antler casting were collected
from male Pere David's deer on Invermay
and live weight and morphological data
were recorded from six male and six female Pere David's deer culled at Woburn
Abbey, Bedford Estates, Bedfordshire, England, in September 1994 when the animals were 15-17 months old.
Results
Hybrid Fertility
The breeding program produced a total of
323 living backcross calves plus 68 nonviable calves (n) (Table 1): 248 (53) from
Al, 48 (5) from natural mating, 19 (6) from
embryo transfer, and 8 (4; 2 singles and 2
twins) born naturally to F, females. Each
of the six F, stags and five F, females mated to red deer produced living progeny,
with the females producing between 1 and
14 backcross progeny (by MOET and natural mating) and the stags between 17 and
170 progeny (by Al and natural mating).
The fertility of the male F, hybrids underpinned the production of the large
herd of hybrids. Pregnancy rates from Al
between years varied from 12-64%. Attempts to freeze and store F, semen were
unsuccessful. Therefore, the success of Al
was highly dependent on the timely collection and quality of fresh semen. The
pregnancy rate for natural mating (36%)
was low compared to red deer (Table 1).
However, there were many mitigating factors; for example in 1992 and 1995 the
breeding sire died of MCF during the
breeding program. Also, from 1993 to
1995, the semen collections were made
from sires during the natural mating program which impaired their performance
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present data on trait variation in the backcross hybrids and discuss the applications of this large hybrid herd to comparative gene mapping, the study of the quantitative trait loci (QTL) which determine
the trait differences between Pere David's
deer and red deer and the genetic improvement of fanned deer.
Table 2. Comparison of traits (mean ± standard deviation) between red deer, W Pere David's deer x
red deer backcross and Pere David's deer
Female
Male
Back
cross
(PD <R)
Gestation length (days)
15 month data"
Body weight (kg)
Skull width (mm)
Skull length (mm)
Metatarsal length
(mm)
Phalange length (mm)
Tall length (mm)
Antler casting date
Back
Pere
cross
(PD X R) David's
deer4
X R
Red deer
X R
Pere
David's
deer*
235 :t 3.4'
247 ± 5 . 3 "
^283
234 ± 3.4' 246 :t 4 . 0 " a. 283
109:t 7.0
164 :t 4.9
355 :t 8.0
125 ii 1 2 "
165 1t 6.1
372 ii 1 3 "
126 ± 10
142 ± 3
369 ± 9
84 ± 5.7
144 ± 4.2
324 ± 10
217 :t 7.9
123 :t 5.4
174 :t 17
2 Nov ± 5 days
222 ii 6.6
134 ii 5.2"
215 i1 2 9 "
9 0ct ± 12 d a y s "
207 ± 5.8
222 ± 4
112 ± 4.9
153 ± 3
150 ± 6.6
312 ± 7
27 July (N = 3)
Red deer
97 :t 8.7" 118 ± 12
144 :t 40 131 ± 3
342 :t 8.2" 352 ± 4
208:t 7.2 214 ± 3
120 :t 4 . 9 " 146 ± 6
184 :t 2 5 " 270 ± 8
with later cycling hinds. The rate of fetal
loss during pregnancy was less than 8% in
both AI and natural mating programs, but
30% after embryo transfer to red deer surrogate dams (Table 1). A high calf death
rate at birth was a feature of all the breeding methods. The dead calves appeared
normal and almost all were full term but
were stillborn. No cause of death on necropsy or postmortem has yet been found.
Traits
The trait measurements from the 1993born cohort are summarized in Table 2.
Data from subsequent years showed similar trends, but the animals were not old
enough to present a full set of comparative measurements. In the 1993 cohort, the
gestational length of the backcross hybrids was 12 days longer than red deer
(Table 2) and the backcross animals were
more variable (a = 5.3 for male calves and
4.0 for females, compared to 3.4 In red
deer). Antler casting dates showed even
larger differences, with the backcross hybrid mean advanced by 24 days from the
red deer mean and the backcross standard
deviation more than twice that of the red
deer (Table 2).
Comparison of the backcross hybrids at
15 months with control red deer (Table 2)
showed that on average the male hybrids
were 16 kg heavier and females 13 kg
heavier than red deer, and the hybrids had
longer heads (1.7 cm in males and 1.8 cm
in females), longer tails (4.1 cm in males
and 3.4 cm in females), and longer feet (1.1
cm in males and 0.8 cm in females). There
were no significant differences in the
length of the metatarsal or in the width of
the head between the hybrids and red
deer. The variance in trait values within
the backcross hybrids was significantly
larger (P < .05) than the red deer controls
for head length (in males), live weight and
tail length. The Pere David's deer used for
comparison in Table 2 were of similar age,
growth stage, and season to the red deer
and backcross animals measured, but
were raised in a different hemisphere under different conditions. Traits that differed between the backcross and red deer
also differed between Pere David's deer
and red deer such that for each of the following ratios the values for Pere David's
deer were greater than hybrids, which
were greater than red deer: head width/
head length, phalange length/metatarsal
length, and live weight/metatarsal length.
Discussion
We have successfully used artificial breeding techniques to generate a total of 391
backcross hybrids between Pere David's
deer and red deer, of which 324 were viable. This hybrid herd is an extraordinary
resource for genetic Investigation because
of the large number of animals and the
fact that genes are segregating which originate from two distinct genomes, previously separated for millions of years. Speciesspecific restriction fragments can be
found in virtually any gene or DNA segment for which Pere David's deer and red
deer are compared (Tate et al. 1995).
Hybrid Fertility and Viability
The breeding program aimed to produce
as many backcross hybrids as possible.
While the success of the breeding program confirms the fertility of hybrids, direct comparisons of fertility between animals and years are confounded by variability in methods and the health and
availability of animals (see Methods). The
only clear factor relating to fertility is that
hybrid semen does not retain motility
when frozen and thawed, whereas frozen
Pere David's deer and red deer semen
were used successfully. Overall, fetal and
perinatal viability, rather than fertility, appear to be the limiting factors in the present experiment and in the other hybrid
breeding programs summarized in Table 1.
The proportion of pregnancies that do not
go to term in red deer hinds is usually
very low, but In hinds carrying 1/4 Pere
David's deer x 3/4 red deer backcross
calves or F, wapiti x red deer calves
about 8% of pregnancies were lost. This
rate increased to 40% In hinds carrying F,
Pere David's deer x red deer calves and
over 80% for F, sambar x red deer hybrid
calves (Table 1). In addition, 17% of the
Pere David's deer backcross calves that
went to term died at birth, while in red
deer, at Invermay, perinatal mortality was
less than 3% in the same years (Pearse AJ,
personal communication). Thus It can be
hypothesized that the success of reproduction in terms of conception, pregnancy, and perinatal death rates are all aspects related to genetic distance between
the parental species in accord with Haldane's hypothesis (1922). Interestingly the
Tate et al • Genetic Analysis of Deer Hybrids 3 6 3
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(PD X R) X R: Progeny of F, Pere David's deer X red deer mated to a red deer. " the backcross mean Is different
from the red deer mean (within sex) at significance level P < .01.
* Measurements at 15 months of age In 15 male and 15 female red deer and 27 male and 39 female backcross animals
born at Invermay In 1993 and 6 male and 6 female Pere David's deer, at 15-17 months of age.
' Pere David's deer data are from various sources; weight and all morphometrics are from animals culled at Woburn
Abbey, Bedfordshire, England. Antler casting data are from two stags at Invermay, and gestation length Is from
Wemmer et al. (1989).
' Data from Fennessy and Mackintosh (1992); N = 52 (male), /V = 34 (female).
These species-specific DNA fragments enable the segregation of Pere David's deer
chromosome segments to be traced in the
backcross and subsequent generations.
The data reported here show that the Pere
David's deer genes have a major influence
on a number of traits. The backcross hybrids are significantly different from the
red deer control groups in gestation
length, antler casting date, growth rate,
head shape, foot size, and tail length. Other studies have shown that backcross hybrids also differ from red deer in neonatal
behavior (Endicott-Davies et al. 1996) and
temperament (Pollard et aJ. 1995). Our ongoing research using this hybrid resource
focuses on two areas, namely constructing
a gene map of deer and testing the relationship between traits and the inheritance of marked chromosome segments.
There is also some limited interest in the
potential of the hybrids as farmed deer.
n=40
n=49
Figure 1. The deer Interspecles backcross reference panel for gene mapping. The panel consists of 89 1/4 Pere
David's deer X 3/4 red deer animals. These are the half-slb progeny ol two F, Pere David's deer X red deer hybrid
sires (GW899 and GW903) mated to 40 and 49 red deer females. The F, sires are themselves the half-slb progeny
of a male Pere David's deer (W294) Circles represent females and squares represent males. The ear tag number
of animals Is noted below. The shading Indicates the proportion of Pere David's deer. The dam of GW899 (Y481)
died before a sample could be taken.
Gene Mapping
We have used the 1/4 Pere David X 3/4 red
deer backcross hybrid pedigrees to build
linkage groups and establish the order of
evolutionarily conserved loci in deer
(Tate et al. 1995). Highly polymorphic microsatellites have also been mapped. However, because the species share alleles, microsatellites are often less informative
than the species-specific restriction fragments detected with gene probes. To date
our data have provided no evidence of recombination suppression or segregation
distortion (Broom et al. 1996; Montgomery et al. 1995; Tate et al. 1995) which is
occasionally seen in the mouse interspecies hybrid pedigrees (Hammer et al.
1989; Siracusa et al. 1989).
To facilitate the construction of the deer
gene map, we have extracted large
amounts of DNA (>5 mg) from 89 backcross progeny and their parents as an international reference panel for deer gene
mapping. The pedigree structure of this
mapping panel is shown in Figure 1. DNA
samples from the panel are available from
the authors. The additional interspecies
hybrid pedigrees reported here are valuable because of the large number of new
meioses which bring the total mapping
panel to 356 backcross individuals. Thus
this resource is unparalleled for determining the fine order of genes in the ruminants (Broom et al. 1996).
3 6 4 The Journal of Heredity 1997:88(5)
Genetic Analysis of Traits
A growing number of studies in domestic
animals have found associations between
marked chromosome segments and variation in quantitative traits (Haley 1995).
One rationale for these experiments is
that the trait differences between artificially selected strains may often be due to
fixation of a few genes with large effects.
In contrast, there are few comparable
studies in natural populations and in general it has been assumed that natural evolution is a more gradual process and that
trait differences between species are likely
to be multlgenic (Falconer 1982; MitchellOlds 1995). The large numbers of Pere David deer hybrids offer a rare opportunity
to test this assertion for a range of traits.
Our aim is to use mapped genetic markers
to determine, in each backcross, which
chromosome segments are inherited from
Pere David's deer and then to test for relationships between inheritance of a particular chromosome segment and variation in specific traits. For several of the
traits examined in this study (e.g., antler
casting date, tail length, and head length),
the backcross animal trait values showed
significantly more variability than red
deer. This is consistent with the hypothesis that segregating Pere David's deer
chromosome segments do not contribute
equally to these traits. If Pere David's deer
chromosome segments are found which
have a major influence on specific traits,
this will challenge the view that evolutionary changes involve numerous loci and,
on farms, may enable us to use genetic
markers to rapidly select hybrid animals
with desirable characteristics.
Evaluation of Hybrids as Fanned Deer
Breeding farmed deer with a more flexible
reproductive seasonally was one of the
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Altmann VD and Scheel H, 1980. Geburt, beginn des
sozialverhaltens und erstes lernen belm Mllu, Elaphurus davktianus. Milu, Berlin 5:146-156.
Asher GW, Adam JL, Otway W, Bowmar P, Van Reenen
Downloaded from http://jhered.oxfordjournals.org/ at Pennsylvania State University on September 17, 2016
sex ratio of all F, Pere David's x red deer
hybrids born was 12 males:14 females,
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of the heterogametlc sex in utero. However, In contrast, the lack of males among
the four sambar deer x red deer hybrids
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initial objectives of Pere David's deer hybridization (Otway 1985) and other hybridization experiments (Muir et al. 1996).
Red deer are highly seasonal breeders,
conceiving in autumn and calving in summer, after the peak spring grass growth period on many New Zealand farms. Pere David's deer typically calve 4-6 weeks earlier, but due to a longer gestation length
(283 compared to 234 days in red deer)
they are conceived 2-3 months earlier
than red deer. The significantly advanced
seasonality of the backcross, as indicated
by the 3 week advancement in mean antler
casting date, suggests the goal of introducing novel variation in seasonality into
farmed herds could perhaps be achieved.
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practical breeding programs is another
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The morphological differences between
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have a direct bearing on farming; for example, features of the Pere David's deer
skull may be related to the fact that this
is one of the few deer species that specifically grazes and will not browse (Bedford
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growth rate is accompanied by a proportionate increase in stature, which has major implications for management of these
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growth and earlier seasonality) which are
valued in farmed deer. Marker-assisted selection may provide a rapid method to introgress these traits into farmed red deer.
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